Phylogenomics and plastome evolution of a Brazilian mycoheterotrophic orchid, Pogoniopsis schenckii

Abstract

Premise Pogoniopsis likely represents an independent photosynthesis loss in orchids. We use phylogenomic data to better identify the phylogenetic placement of this fully mycoheterotrophic taxon, and investigate its molecular evolution. Methods We performed likelihood analysis of plastid and mitochondrial phylogenomic data to localize the position of Pogoniopsis schenckii in orchid phylogeny, and investigated the evolution of its plastid genome. Results All analyses place Pogoniopsis in subfamily Epidendroideae, with strongest support from mitochondrial data, which also place it near tribe Sobralieae with moderately strong support. Extreme rate elevation in Pogoniopsis plastid genes broadly depresses branch support; in contrast, mitochondrial genes are only mildly rate elevated and display very modest and localized reductions in bootstrap support. Despite considerable genome reduction, including loss of photosynthesis genes and multiple translation apparatus genes, gene order in Pogoniopsis plastomes is identical to related autotrophs, apart from moderately shifted inverted repeat (IR) boundaries. All cis‐spliced introns have been lost in retained genes. Two plastid genes (accD, rpl2) show significant strengthening of purifying selection. A retained plastid tRNA gene (trnE‐UUC) of Pogoniopsis lacks an anticodon; we predict that it no longer functions in translation but retains a secondary role in heme biosynthesis. Conclusions Slowly evolving mitochondrial genes clarify the placement of Pogoniopsis in orchid phylogeny, a strong contrast with analysis of rate‐elevated plastome data. We documented the effects of the novel loss of photosynthesis: for example, despite massive gene loss, its plastome is fully colinear with other orchids, and it displays only moderate shifts in selective pressure in retained genes.

Plastid phylogenomics and molecular evolution of Thismiaceae (Dioscoreales)

“…However, the endoholoparasites Pilostyles aethiopica (Apodanthaceae), P. hamiltonii (Apodanthaceae), and Rafflesia lagascae (Rafflesiaceae) have plastid genomes completely lacking trnE genes (or in the case of R. lagascae potentially no plastid genome) (Molina et al, 2014; Bellot and Renner, 2015). In addition, plastid genomes of holoparasitic Balanophora reflexa and B. laxiflora (Balanophoraceae; Su et al, 2019) and the fully mycoheterotrophic orchid Pogoniopsis schenckii (Klimpert et al, 2022) appear to have pseudogenized copies of trnE‐UUC with respect to their function in protein synthesis; the plastid genomes of several other taxa in Balanophoraceae also lack trnE (Ceriotti et al, 2021).…”

“…| 19 of 25 and B. laxiflora (Balanophoraceae; Su et al, 2019) and the fully mycoheterotrophic orchid Pogoniopsis schenckii (Klimpert et al, 2022) appear to have pseudogenized copies of trnE-UUC with respect to their function in protein synthesis; the plastid genomes of several other taxa in Balanophoraceae also lack trnE (Ceriotti et al, 2021).…”

Plastid genome evolution in leafless members of the orchid subfamily Orchidoideae, with a focus onDegranvillea dermaptera

“…Degranvillea) and thus genes with Group IIA introns are transcribed and translated, somehow remaining functional; 5) these genes are transcribed but result in non-functional products; or 6) they are not transcribed at all, and may be effectively considered pseudogenes (Zoschke et al, 2010;Delannoy et al, 2011;Naumann et al, 2016;Graham et al, 2017). The situation in the epidendroid orchid Pogoniopsis schenckii (Klimpert et al, 2022), which has lost both matK and all Group IIA introns (as might be expected given the loss of matK), may represent what the future holds for Degranvillea, with the latter representing an intermediate stage in plastome reduction, considering gene-gene product interactions. A similar situation is observed among several species of Gastrodia and the related Didymoplexis pallens which have lost matK (independently within tribe Gastrodieae Lindl.)…”

Phylotranscriptomic Analyses of Mycoheterotrophic Monocots Show a Continuum of Convergent Evolutionary Changes in Expressed Nuclear Genes From Three Independent Nonphotosynthetic Lineages

“…Fully mycoheterotrophic monocots have also experienced losses of most plastid genes except some housekeeping genes ( Petersen et al 2018 ) and core bioenergetic genes ( Lam et al 2018 ). However, the long-term retention of one or more non-bioenergetic genes and bifunctional trnE (which is involved in heme biosynthesis in addition to its role in plastid translation) may explain the long-term evolutionary retention of the plastid genome (e.g., Graham et al 2017 ; Klimpert et al 2022 ). In both parasitic and mycoheterotrophic species, plastome degradation in heterotrophic plants is typically associated with the elevation of nucleotide substitutions ( McNeal et al 2007 ; Lam et al 2015 ; Feng et al 2016 ; Wicke et al 2016 ; Barrett et al 2018 ), genomic rearrangements, decrease in GC content, and sporadic weakening of purifying selection (e.g., Wicke et al 2016 ; Barrett et al 2018 ; Joyce et al 2018 ), although not all of these phenomena have been reported in all cases.…”

“…Still, plastomes may not always be the best candidates to be used for phylogenomic estimates of mycoheterotrophic or parasitic plants because the photosynthesis genes may be lost or evolving very rapidly relative to other lineages, potentially yielding misleading results ( Lam et al 2018 ). By contrast, the use of mitochondrial genomes, whose genes are both slowly evolving in general and less rate-elevated in mycoheterotrophic lineages in particular, can help place lineages that are susceptible to long-branch attraction issues for plastid data (e.g., Merckx, Bakker, et al 2009 ; Klimpert et al 2022 ; Lin et al 2022 ).…”